Assessment of biochemical and immunomodulatory activity of sulphated polysaccharides from Ulva intestinalis

International Journal of Biological Macromolecules

Volumn 91, Issue , 2016, Pages 269-277

  Peasura, Napassorn ^a   Laohakunjit, Natta ^a   Kerdchoechuen, Orapin ^a   Vongsawasdi, Punchira ^a   Chao, Louis Kuoping ^b  

^a KING MONGKUT'S UNIVERSITY OF TECHNOLOGY THONBURI   (Thailand)

^b CHINA MEDICAL UNIVERSITY   (Taiwan)

Author keywords

Immunomodulatory activity; Silica silica column; Sulphated polysaccharide; Ulva intestinalis

Indexed keywords

1,1 DIPHENYL 2 PICRYLHYDRAZYL; CARBOHYDRATE; INTERLEUKIN 1BETA; NITRIC OXIDE; POLYSACCHARIDE SULFATE; SULFATE; TUMOR NECROSIS FACTOR ALPHA; IMMUNOLOGIC FACTOR; MONOKINE; POLYSACCHARIDE;

ANIMAL CELL; ANTIOXIDANT ACTIVITY; ARTICLE; BIOCHEMISTRY; CONTROLLED STUDY; DRUG EFFECT; DRUG MECHANISM; IMMUNOMODULATION; MACROPHAGE; MOLECULAR DYNAMICS; MOLECULAR WEIGHT; MOUSE; NONHUMAN; STRUCTURE ANALYSIS; ULVA; ULVA INTESTINALIS; ANIMAL; CELL LINE; CHEMISTRY; IMMUNOLOGY; METABOLISM;

ANIMALS; CELL LINE; IMMUNOLOGIC FACTORS; MACROPHAGES; MICE; MONOKINES; NITRIC OXIDE; POLYSACCHARIDES; ULVA;

EID: 84973495966     PISSN: 01418130     EISSN: 18790003     Source Type: Journal    
DOI: 10.1016/j.ijbiomac.2016.05.062     Document Type: Article

References (64)

1. Kim J.-K., Cho M.L., Karnjanapratum S., Shin I.-S., You S.G. In vitro and in vivo immunomodulatory activity of sulfated polysaccharides from Enteromorpha prolifera. Int. J. Biol. Macromol. 2011, 49(5):1051-1058.
2. Pérez-Recalde M., Matulewicz C.M., Pujol A.C., Carlucci J.M. In vitro and in vivo immunomodulatory activity of sulfated polysaccharides from red seaweed Nemalion helminthoides. Int. J. Biol. Macromol. 2014, 63:38-42.
3. Percival E. The polysaccharides of green, red and brown seaweeds: their basic structure, biosynthesis and function. Brit. Phycol. J. 1979, 14:103-117.
4. Tabarsa M., Lee S.-J., You S.G. Structural analysis of immunostimulating sulfated polysaccharides from Ulva pertusa. Carbohyd. Res. 2012, 361(1):141-147.
5. Ray B. Polysaccharides from Enteromorpha compressa: Isolation, purification and structural features. Carbohyd. Polym. 2006, 6:408-416.
6. Peasura N., Laohakunjit N., Kerdchoechuen O., Wanlapa S. Characteristics and antioxidant of Ulva intestinalis sulphated polysaccharides extracted with different solvents. Int. J. Biol. Macromol. 2015, 81:912-919.
7. Coste O., Malta E.-J., López J.C., Fernández-Díaz C. Production of sulfated oligosaccharides from the seaweed Ulva sp. using a new ulvan-degrading enzymatic bacterial crude extract. Algal Res. 2015, 10:224-231.
8. Castro R., Piazzon M.C., Zarra I., Leiro J., Noya M., Lamas J. Stimulation of turbot phagocytes by Ulva rigida C. Agardh polysaccharides. Aquaculture 2006, 254:9-20.
9. Park S., Nahm M.H. L-rhamnose is often an important part of immunodominant epitope for pneumococcal serotype 23f polysaccharide antibodies in human sera immunized with ppv23. PLoS One 2013, 8:1-6.
10. Wang L., Li X.X., Chen Z.X. Sulfated modification of the polysaccharides obtained from defatted rice bran and their antitumor activities. Int. J. Biol. Macromol. 2009, 44:211-214.
11. Malyshev I.Y., Manukhina E.B., Malyshev Y.I. Physiological organization of immune response based on the homeostatic mechanism of matrix reprogramming: implication in tumor and biotechnology. Med. Hypotheses 2014, 82(6):754-765.
12. Leiro J.M., Castro R., Arranz J.A., Lamas J. Immunomodulating activities of acidic sulphated polysaccharides obtained from the seaweed Ulva rigida C. Agardh. Int. Immunopharmacol. 2007, 7:879-888.
13. Lee J.B., Ohta Y., Hayashi K., Hayashi T. Immunostimulating effects of a sulfated galactan from Codium fragile. Carbohyd. Res. 2010, 345:1452-1454.
14. Karnjanapratum S., Tabarsa M., Cho M., You S.G. Characterization and immunomodulatory activities of sulfated polysaccharides from Capsosiphon fulvescens. Int. J. Biol. Macromol. 2012, 51:720-729.
15. Paul A., Pendreigh R.H., Plevin R. Protein kinase C and tyrosine kinase pathways regulate lipopolysacchride-induced nitric oxide synthase activity in RAW 264.7 macrophages. Br. J. Pharmacol. 1995, 114:482-488.
16. Li C., Huang Q., Fu X., Yue X.J., Liu R.H., You L.J. Characterization, antioxidant and immunomodulatory activities of polysaccharides from Prunella vulgaris Linn. Int. J. Biol. Macromol. 2015, 75:298-305.
17. Karnjanapratum S., You S. Molecular characteristics of sulfated polysaccharides from Monostroma nitidum and their in vitro anticancer and immunomodulatory activities. Int. J. Biol. Macromol. 2011, 48:311-318.
18. Dubois M., Gilles K.A., Hamilton J.K., Rebers P.A., Smith E. Colorimetric method for determination of sugars and related substances. Anal. Chem. 1956, 28:350-356.
19. Lloyd A.G., Dodgson K.S., Price R.G., Rose F.A.I. Infrared studies on sulphate esters. I. Polysaccharide sulphates. Biochim. Biophys. Acta 1961, 46:108-115.
20. Schoniger W. A rapid micro-analytical determination of halogen in organic substances. Microchim. Acta. 1955, 1:123-129.
21. Wang Q., Wood P.J., Huang X., Cui W. Preparation and characterization of molecular weight standards of low polydispersity from oat and barley (1/3) (1/4)-β-d-glucan. Food Hydrocolloids 2003, 17:845-853.
22. Shimada K.K., Fujikawa K., Yahara K., Nakamura T. Antioxidative properties of xanthan on the autoxidation of soybean oil in cyclodextrin emulsion. J. Agric. Food. Chem. 1992, 40:945-948.
23. Shin K.S., Kwon N.J., Kim Y.H., Park H.S., Kwon G.S., Yu J.H. Differential roles of the ChiB chitinase in autolysis and cell death of Aspergillus nidulans Eukaryot. Cell 2009, 8:738-746.
24. Zhang L., Koyyalamudi S.R., Jeong S.C., Reddy N., Smith P.T., Ananthan R., Longvah T. Antioxidant and immunomodulatory activities of polysaccharides from the roots of Sanguisorba officinalis. Int. J. Biol. Macromol. 2012, 51(5):1057-1062.
25. Green L.C., Wanger D.A., Glogowski J., Skipper P.L., Wishnok J.S., Tannenbaum S.R. Analysis of nitrate, nitrite and nitrate in biological fluids. Anal. Biochem. 1982, 126:131-138.
26. Zhang L., Ravipati A.S., Shanmugam K., Munch G., Koyyalamudi S.R., Jeong S.C., Reddy N., Smith P., Bartlett J., Wu M.J. Antioxidant and anti-inflammatory activities of selected medicinal plants containing phenolic and flavonoid compounds. J. Agric. Food Chem. 2011, 59:12361-12367.
27. Zhuravlev L.T. The surface chemistry of amorphous silica. Zhuravlev model. Colloids Surf. A 2000, 173:1-38.
28. Veeraperumal S., Chinnathambi A., Perumal P., Ramasamy R. Protective effect of Ulvan from Ulva lactuca against experimentally induced fibrosarcoma in wistar rats. Int. J. Curr. Sci. 2012, 4:50-56.
29. Jayakumar R., Nwe N., Tokura S., Tamura H. Sulfated chitin and chitosan as novel biomaterials. Int. J. Biol. Macromol. 2007, 40:175-181.
30. Biermann J.C., McGinnis D.G. Analysis of carbohydrates by GLC and MS. High-performance Liquid Chromatography (HPLC) of Carbohydrates 1988, 19-24. CRC Press, New jersey. D.G. McGinnis, L.M. Laver, J.C. Biermann (Eds.).
31. Rodríguez-Jasso R.M., Mussatto S.I., Pastrana L., Aguilar C.N., Teixeria J.A. Extraction of sulfated polysaccharides by autohydrolysis of brown seaweed Fucus vesiculosus. J. Appl. Phycol. 2012, 25(1):31-39.
32. Shao P., Chen X., Sun P. In vitro antioxidant and antitumor activities of different sulfated polysaccharides isolated from three algae. Int. J. Biol. Macromol. 2013, 62:155-161.
33. Costa C., Alves A., Pinto P.R., Sousa R.A., Borges da Silva E.A., Reis R.L., Rodrigues A.E. Characterization of ulvan extracts to assess the effect of different steps in the extraction procedure. Carbohyd. Polym. 2012, 88:537-546.
34. Fareeha A., Atika A., Aliya R. Protein extraction from Ulva lactuca and Padina pavonica found at Buleji coast Karachi, Pakistan. Int. J. Phycol. Phycochem. 2013, 9:49-52.
35. Costa L.S., Fidelis G.P., Cordeiro S.L., Oliveira R.M., Sabry D.A., Camara R.B.G., Nobre T.D.B., Costa M.S.S.P., Almeida-Lima J., Farias E.H.C., Leite E.L., Rocha H.A.O. Biological activities of sulfated polysaccharides from tropical seaweeds. Biomed. Pharmacother. 2010, 64:21-28.
36. Jiao Y., Wickett N.J., Ayyampalayam S., Chanderbali A.S., Landherr L., Ralph P.E., Tomsho L.P., Hu Y., Liang H., Soltis P.S., Soltis D.E., Clifton S.W., Schlarbaum S.E., Schuster S.C., Ma H., Leebens-Mack J., De Pamphilis C.W. Ancestral polyploidy in seed plants and angiosperms. Nature 2011, 473:97-100.
37. Alekseeva A., Casu B., Torri G., Pierro S., Naggi A. Profiling glycol-split heparins by high-performance liquid chromatography/mass spectrometry analysis of their heparinase-generated oligosaccharides. Anal. Biochem. 2013, 434:112-122.
38. Xu J., Xu L.L., Zhou Q.W., Hao S.X., Zhou T., Xie H.J. Isolation purification, and antioxidant activities of degraded polysaccharides from Enteromorpha prolifera. Int. J. Biol. Macromol. 2015, 81:1026-1030.
39. Lai F., Wen Q., Li L., Wu H., Li X. Antioxidant activities of water-soluble polysaccharide extracted from mung bean (Vigna radiata L.) hull with ultrasonic assisted treatment. Carbohyd. Polym. 2010, 81(2):323-329.
40. Qi H.M., Zhao T.T., Zhang Q.B., Li Z., Zhao Z.Q., Xing R. Antioxidant activity of different molecular weight sulfated polysaccharides from Ulva pertusa Kjellm (Chlorophyta). J. Appl. Phycol. 2005, 17:527-534.
41. Wang J., Zhang Q.B., Zhang Z.S., Li Z. Antioxidant activity of sulfated polysaccharide fractions extracted from Laminaria japonica. Int. J. Biol. Macromol. 2008, 42:127-132.
42. Liu C., Lu J., Lu L., Liu Y., Wang F., Xiao M. Isolation: structural characterization and immunological activity of an exopolysaccharide produced by Bacillus licheniformis 8-37-0-1. Bioresour. Technol. 2010, 101:5528-5533.
43. De Felice C., Ciccoli L., Leoncini S., Signorini C., Rossi M., Vannuccini L., Guazzi G., Latini G., Comporti M., Valacchi G., Hayek J. Systemic oxidative stress in classic Rett syndrome. Free Radical Biol. Med. 2009, 47(4):440-448.
44. Toledo C.E.P., Souza M.A., Fraga M.R., Ribeiro L.C., Ferreira A.P., Vitral R.W.F. Cellular viability and nitric oxide (NO) production by J774 macrophages in the presence of orthodontic archwires. J. Biomed. Sci. Eng. 2012, 5:255-262.
45. Veremeichenko S.N., Zdorovenko G.M. Specific structural features and immunomodulatory properties of the lipopolysaccharides of Pseudomonas bacteria. Appl. Biochem. Microbiol. 2008, 44(6):571-579.
46. Liu B., Wang K., Gao H.M., Mandavilli B., Wang J.Y., Hong J.S. Molecular consequences of activated microglia in the brain: over activation induces apoptosis. J. Neurochem. 2001, 77:182-189.
47. Liew F.Y. Interactions between cytokines and nitric oxide. Adv. Neuroimmunol. 1995, 5:201-209.
48. Miao H., Yuan S., Wang Y., Tsygankov A., Chien S. Role of cbl in shear-Activation of PI 3-Kinase and JNK in endothelial cells. Biochem. Biophys. Res. Commun. 2002, 292:892-899.
49. Akira S., Takeda K. Toll-like receptor signaling. Nat. Rev. Immunol. 2004, 4:499-511.
50. Karin M. The beginning of the end: iκB kinase (IKK) and NF-κB activation. J. Biol. Chem. 1999, 274:27339-27342.
51. Bao J., Lu Z., Joseph J.J., Carabenciov D., Dimond C.C., Pang L., Samsel L., McCoy J.P., Leclerc J., Nguyen P., Gius D., Sack M.N. Characterization of the murine SIRT3 mitochondrial localization sequence and comparison of mitochondrial enrichment and deacetylase activity of long and short SIRT3 isoforms. J. Cell. Biochem. 2010, 110:238-247.
52. Suárez E.R., Syvitski R., Kralovec J.A., Noseda M.D., Barrow C.J., Ewart H.S., Lumsden M.D., Grindley T.B. Immunostimulatory polysaccharides from Chlorella pyrenoidosa. A new galactofuranan measurement of molecular weight and molecular weight dispersion by DOSY NMR. Biomacromolecules 2006, 7:2368-2376.
53. Maeda R., Ida T., Inara H., Sakamoto T. Immunostimulatory activity of polysaccharides isolated from Caulerpa lentillifera on macrophage cells. Biosci. Biotechnol. Biochem. 2012, 76:501-505.
54. Alkhatib B., Freguin-Bouilland C., Lallemand F., Henry J.P., Litzler P.Y., Marie J.P., Richard V., Thuillez C., Plissonnier D. Low molecular weight fucan prevents transplant coronaropathy in rat cardiac allograft model. Transpl. Immunol. 2006, 16:14-19.
55. Baugh J.A., Bucala R. Mechanisms for modulating TNF alpha in immune and inflammatory disease. Curr. Opin. Drug Discov. 2001, 4(5):635-650.
56. Chen Y., Zhang H., Wang Y., Nie S., Li C., Xie M. Sulfated modification of the polysaccharides from Ganoderma atrum and their antioxidant and immunomodulating activities. Food Chem. 2015, 186:231-238.
57. Lake A.C., Vassy R., Benedetto M.D., Lavigne D., Visage C.L., Perret G.Y., Letourneur D. Low molecular weight fucoidan increases VEGF165-induced endothelial cell migration by enhancing VEGF165 binding to VEGFR-2 and NRP1. J. Biol. Chem. 2006, 281:37844-37852.
58. Miao B., Li J., Fu X., Ding J., Geng M. T-cell receptor (TCR)/CD3 is involved in sulfated polymannuroguluronate (SPMG)-induced T-lymphocyte activation. Int. Immunopharmacol. 2005, 5:1171-1182.
59. Miao B., Geng M., Li J., Li F., Chen H., Guan H., Ding J. Sulfated polymannuroguluronate a novel anti-acquired immune deficiency syndrome (AIDS) drug candidate, targeting CD4 in lymphocytes. Biochem. Pharmacol. 2004, 68:641-649.
60. Tidball J.G., Villalta S.A. Nitric oxide may prompt calcium leakage in dystrophic muscle. Nat. Med. 2009, 15:243-244.
61. Holderness J., Schepetkin I.A., Freedman B., Kirpotina L.N., Quinn M.T., Hedges J.F., Jutila M.A. Polysaccharides isolated from Acai fruit induce innate immune responses. PLoS One 2011, 6(2):1-14.
62. Le J., Vilcek J. Tumor necrosis factor and interleukin 1: cytokines with multiple overlapping biological activities. Lab. Invest. 1987, 56:234-248.
63. Beutler B., Cerami A. Tumor necrosis, cachexia, shock, and inflammation: a common mediator. Annu. Rev. Biochem. 1988, 57:505-518.
64. Schepetkin I.A., Quinn M.T. Botanical polysaccharides: macrophage immunemodulation and therapeutic potential. Int. Immunopharmacol. 2006, 6:317-333.